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An atlas of anterior hox gene expression in the embryonic sea lamprey head: hox-code evolution in vertebrates

Parker, Hugo J. and Bronner, Marianne E. and Krumlauf, Robb (2019) An atlas of anterior hox gene expression in the embryonic sea lamprey head: hox-code evolution in vertebrates. Developmental Biology, 453 (1). pp. 19-33. ISSN 0012-1606. PMCID PMC6667299. https://resolver.caltech.edu/CaltechAUTHORS:20190311-132253895

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Abstract

In the hindbrain and the adjacent cranial neural crest (NC) cells of jawed vertebrates (gnathostomes), nested and segmentally-restricted domains of Hox gene expression provide a combinatorial Hox-code for specifying regional properties during head development. Extant jawless vertebrates, such as the sea lamprey (Petromyzon marinus), can provide insights into the evolution and diversification of this Hox-code in vertebrates. There is evidence for gnathostome-like spatial patterns of Hox expression in lamprey; however, the expression domains of the majority of lamprey hox genes from paralogy groups (PG) 1–4 are yet to be characterized, so it is unknown whether they are coupled to hindbrain segments (rhombomeres) and NC. In this study, we systematically describe the spatiotemporal expression of all 14 sea lamprey hox genes from PG1-PG4 in the developing hindbrain and pharynx to investigate the extent to which their expression conforms to the archetypal gnathostome hindbrain and pharyngeal hox-codes. We find many similarities in Hox expression between lamprey and gnathostome species, particularly in rhombomeric domains during hindbrain segmentation and in the cranial neural crest, enabling inference of aspects of Hox expression in the ancestral vertebrate embryonic head. These data are consistent with the idea that a Hox regulatory network underlying hindbrain segmentation is a pan vertebrate trait. We also reveal differences in hindbrain domains at later stages, as well as expression in the endostyle and in pharyngeal arch (PA) 1 mesoderm. Our analysis suggests that many Hox expression domains that are observed in extant gnathostomes were present in ancestral vertebrates but have been partitioned differently across Hox clusters in gnathostome and cyclostome lineages after duplication.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.ydbio.2019.05.001DOIArticle
https://doi.org/10.1101/571448DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6667299/PubMed CentralArticle
ORCID:
AuthorORCID
Parker, Hugo J.0000-0001-7646-2007
Bronner, Marianne E.0000-0003-4274-1862
Krumlauf, Robb0000-0001-9102-7927
Alternate Title:Hox code in lamprey head development
Additional Information:© 2019 Elsevier Inc. Received 26 February 2019, Revised 5 April 2019, Accepted 1 May 2019, Available online 6 May 2019. We thank Stephen Green, Dorit Hockman, Tetsuto Miyashita, and Megan Martik for lamprey husbandry assistance, and the Stowers Institute Histology facility for sectioning assistance. HJP and RK were supported by the Stowers Institute (RK grant #2013-1001). MEB was supported by grants RO1NS108500 and R35 NS111564.
Funders:
Funding AgencyGrant Number
Stowers Institute for Medical ResearchRK 2013-1001
NIHR01 NS108500
NIHR35 NS111564
Subject Keywords:Hox expression; Hindbrain segmentation; Cranial neural crest; Vertebrate evolution; Rhombomeres; Lamprey; Gene regulation; Axial patterning
Issue or Number:1
PubMed Central ID:PMC6667299
Record Number:CaltechAUTHORS:20190311-132253895
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190311-132253895
Official Citation:Hugo J. Parker, Marianne E. Bronner, Robb Krumlauf, An atlas of anterior hox gene expression in the embryonic sea lamprey head: Hox-code evolution in vertebrates, Developmental Biology, Volume 453, Issue 1, 2019, Pages 19-33, ISSN 0012-1606, https://doi.org/10.1016/j.ydbio.2019.05.001. (http://www.sciencedirect.com/science/article/pii/S0012160619301265)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:93686
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:11 Mar 2019 21:14
Last Modified:03 Oct 2019 20:56

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